MARINE ECOLOGY PROGRESS SERIES Vol. 134: 119-130, 1996 Published April 25 Mar Ecol Prog Ser l

Effects of macrobenthic burrows on infaunal communities in tropical tidal flats

Sabine Dittmann*

Zentrum fiir Marine Tropenokologie, Fahrenheitstr. 1, D-28359 Bremen, Germany

ABSTRACT The effects of burrows on the infaunal community In a tropical t~dalflat were studied on the northeast coast of . A comparative survey of infauna In burrows versus adjacent sediment was carr~edout for the burrows of 3 (Scopimera inflata, Uca spp.. Callianassa austrahensis) and a brachiopod (Llngula anatjna). More (1.5 to 2.5~)infauna occurred within burrows than in adja- cent sediments Densities of meiobenthic , copepods and Platyhelminthes were significantly higher wlthin the burrows of Uca spp., C. australiensis and L. anatina. In the latter 2 cases multivariate analyses showed distinct communities in burrows and adjacent sediment, although this was not con- sistent over time for the brachiopod burrows. No differences in community composition were detected in the cases of Uca spp. and S. inflata. In a field experiment. C. austral~ensiswas excluded from 7 sites, and infaunal abundances and compositions were followed for 1 yr and compared with control sites. From the very beginning, me~ofaunaldensities were significantly lower in the exclusion sites, mainly due to reduced densities of nematodes and copepods. The effect of the shrimp exclus~onon macrofauna was less pronounced, but after 1 yr total numbers of macrofauna were significantly lower in the exclusions, due to the distribution of amphipods. The results showed that promotive interactions play an important role in structuring tropical tldal flat communities.

KEY WORDS: Benthos communities . Burrows . Callianassa . Field experiments Meiofauna . Promo- tlve interaction . Tropical tidal flat

INTRODUCTION 1985, Branch & Pnngle 1987) The effects of biogenic structures have also been discussed in the light of Biogenic structures of benthlc organisms have been various functional-mode hypotheses (Rhoads & Young shown to have contrasting effects on infauna. On the 1970, Woodin 1976, Murphy 1985, Posey 1986, 1987, one hand, macrobenthic burrows may enhance the Dittmann 1990). presence of smaller infauna by providing suitable For tropical tidal flats, ambiguous accounts exist on microhabitats in sediment depth, where they would the relevance of biotic interactions for structuring otherwise not be able to live (Bell et al. 1978, Reise benthic communities. Sanders (1968) took tropical 1981, 1987, Meyers et al. 1987, Schaffner 1990). This shallow-water marine regions as an example of bio- process, termed accommodation, is one of the major logically accommodated communities, whereas Moore promotive interactions structuring benthic communi- (1972) and Alongi (1987, 1990) argued that the high ties (Reise 1985). Macrobenthos tubes can provide physical stress in tropical marine environments out- refuge from or facilitate larval settlement weighs biological processes in regulating intertidal (Woodin 1978, Bell & Woodin 1984, Bell 1985). On the populations. The existence of commensals associated other hand, infaunal abundances can be reduced in with intertidal macrobenthos has been reported from assemblages of burrowing organisms, an effect often the tropics (Kenway 1981, Morton & Morton 1983), yet attributed to bioturbation (Brenchley 1981, Murphy no quantitative study has been carried out to assess the - relevance of biogenic structures for the benthic com- 'Present E-mall [email protected]_wilhelmshaven.de munity in tropical tidal flats.

0 Inter-Research 1996 Resale of full art~clenot permitted Mar Ecol Prog Ser 134. 119-130, 1996

The aim of this investigation was to study whether MATERIALS AND METHODS burrows of macrobenthic organisms affect densities and/or species composition of smaller infauna in a The investigation was carried out between 1988 and tropical tidal flat. Decapod crustaceans are among the 1991 on the tropical northeast coast of Australia. Here, dominant macrobenthos dwellers in tropical tidal flats tidal flats extend along estuaries and bays and often (Rcise 1985, 1991, Alongi 1990, Dittmann 1995) and occur on the seaward side of mangrove forests. Tidal several burrowing crustaceans were chosen for this ranges are 2 to 2.5 m on average (Dittmann 1995). study. the sand bubbler Scopimera inflata Milne Assemblages of the brachiopod Lingula anatina and Edwards, 1873, fiddler of the genus Uca, and the burrows of Scopimera inflata were studied in Hinchin- shrimp Callianassa australiensis (Dana). In addition, brook Channel; all other studies were carried out in dense patches of brachiopods (Lingula anatina La- the Haughton Estuary (Fig. 1). The sediment at the marck) were chosen as a further representative of studied sites consisted of fine sand (median grain size tropical macrobenthos. Densities of L. anatina on the 0.19 * 0.05 mm; sorting coefficient 1.59 + 0.34) with a Queensland coast, Australia, exceed 100 ind, m-' medium to low organic matter content [mud bank with (Kenchington & Hammond 1978). The hypothesis flddler crabs: 2.97% dry wt (DW); muddy sand flats: tested was that burrows increase infaunal abundances 1.38% DW]. and species numbers. To test this hypothesis, both a For a comparative survey, sediment samples were comparative study on infauna in burrows versus adja- taken from burrows of ocypodid crabs (Scopimera inflata cent sediment and an experiment in which C. aus- and Uca spp.), Lingula anatina and Callianassa aus- traliensis was excluded were carried out. traliensis, and compared with ambient sediment sam- The burrows of Callianassa australiensis extend over ples. These macrobenthic species occurred in different 1 m in depth and resin casts showed that the U-shaped communities (Dittrnann 1995, unpubl.). In each case, 5 or top part of the burrow merges at about 20 cm depth to 6 random samples were taken from burrows and the a single vertical tunnel that forms a branched network same number of replicates was taken from, the sediment of tunnels with horizontal chambers at over 50 cm surface adjacent (at least 1 cm distance) to burrows, all depth (Kenway 19811. On the surface, one of the open- within areas of 10 m2 The corers used for each burrow ings has a small cone-shaped mound c1 cm in eleva- type had a cross section just wide enough to include 2 to tion and is thus negligible in comparison to mounds of 5 mm of the sediment lining the respective burrow. Sam- other thalassinidean shrimps, which can reach eleva- ples were taken to a depth of 5 cm, and a lower horizon tions up to 1 m above the sediment surface (Griffis & (5 to 10 cm depth) was additionally sampled in burrows Suchanek 1991); the other opening has no mound. This of L. anatina to consider the effect of burrows on the burrow type represents a combination of burrow types vertical distribution of meiofauna in the sediment. 4 and 5 as classified by Griffis & Suchanek (1991). These authors specify shrimps of these types as filter/ suspension feeders, whereas Kenway (1981) describes the feeding process of C. australiensis as sand-sifting and showed that they feed while burrowing. This does not imply that material suspended while digging can- not be trapped on plumose setae on the antennae. inchinbrook In several temperate and subtropical locations, stud- ies have examined the effect of thalassinidean burrows on sediment reworking (Suchanek 1983, Suchan.ek & Colin 1986), microgeochemistry and microbial activi- ties (Aller et al. 1983, Dobbs & Guckert 1988) and infaunal abundances (Peterson 1977, Alongi 1986, Posey 1986, Branch & Pringle 1987, Posey et al. 1991). So far the studies have shown that the shrimp burrows provide a rich microbial and microalgal food source, but bioturbating activities exclude certain infauna spe- cies or functional modes. The results of the present investigation are discussed in relation to burrow type, effects of burrows reported from tidal flats elsewhere and previous accounts of communi.ty composition in beds of thalasslnidean Fig. 1. Northeast coast of Australia, show~ngthe location of shrimps. the study areas D~ttmannMacrobenthic burrows in trop~calt~dal flats

Meiofauna was extracted by repeated shaking and layers of flyscreen (mesh size 1 5 mm) were implanted decantation through a set of sieves of 125, 80 and into the sediment at 7 of the sites before the sediment 40 pm mesh size. The samples were diluted with sea- was replaced in its oliginal position At the other 7 water, following narcotization with MgC1,. All sedi- sites, the sediment was ~eplacedwithout implanting ment samples were treated alive. screens and thus served as controls To aid in locating To study the effect of burrows of Callianassa aus- the sites, sticks were put into the sediment along the traliensis on community composition, an exclusion ex- site margins The arrangement of the sites was chosen periment was designed following the approach used haphazardly, making su~ethat the treatments were by Reise (1983) to exclude Arenlcola rnarlna from a inte~spersed Distances between sites were at least temperate tidal flat. C. australlensls is the structuring 2 m The flyscieen was effective in inhibiting the organism in the muddy sandflat of the studied inter- mobility of the shrlmps which could no longer reach tidal area (Dittmann 1995), and as ambient communi- the surface to irrigate their burrows and so moved ties differed in their sedimentological parameters, the away (Fig 2) experiment had to be carried out within the community The experiment was set up on 11 July 1989 and by creating sites without shrimps. This was achieved sampled after 1, 6, 11, 18 and 53 wk The repetitive as follows. At 14 sites of 75 X 75 cm area each, the sampling of the sites caused negligible disturbance sediment was carefully lifted off to a depth of 5 cm with The sediment volume removed per site on each sam- a shovel and placed on a plastic panel. Horizontal pling occasion amounted to 280 cm3, equivalent to l %

Fig 2 Expenmental treatments 1 \vk after their estabhshment (a) control slte, (b) exclusion of Callianassa aus- traljensis See 'Matenals and methods for details Each site was 0 56 m2 in area 122 Mar Ecol Prog Ser 134: 119-130, 1996

of the sediment volume of each site. Meiofaunal sam- age from Plymouth Marine Laboratory (UK). Multi- ples were taken with a corer of 3.69 cm2 surface area. variate analyses were carried out on untransformed Three samples were taken from each site and com- data using the Bray-Curtis index and the group aver- bined in the field to 1 sample per site. On the flrst 3 age linkage method for cluster analysis and non-metric sampling dates, the samples were divided into hori- multidimensional scaling (MDS) ordmation. Sites (bur- zons of 0-1 and 1-5 cm sediment depth. The samples rows vs adjacent sediment) or treatments were dis- were processed as described above. For macrofauna, criminated by 2-way nested ANOSIM (Clarke 1993), samples were taken with a 15 cm2 corer to a sed~ment testing the null hypothesis that no differences existed depth of 5 cm. They were sieved through 0.25 mm between sites or treatments. mesh. Corer and sieve size were adjusted to the small individual sizes of macrobenthos in the study area (Dittmann 1995). Again, 3 samples from each site were RESULTS combined to form 1 sample per site. This combination of replicates of experimental sites is 'sacrificial pseudo- Comparative survey of burrows and adjacent sediment replication' sensu Hurlbert (1984). An analysis of within-site variability was omitted, as a maximization In the studied tidal flats, nematodes accounted on of treatment sites was considered to be most important average for 75% of the permanent meiofauna, fol- and samples had to be processed quickly. lowed by copepods at 15 %, Platyhelminthes at 5 % and In November 1989, one each of the exclusion and ostracods at 2 %. Further taxa encountered frequently control sites was lost due to disturbance by stingrays. but in low numbers were Halacarida, Kinorhynchia, In early 1990 heavy monsoonal activity caused flood- Tardigrada, Gastrotricha and Gnathostomulida. ing of the estuary. In samples taken right after the Results of the comparison of infauna inside and out- floods in April 1990 almost no were encoun- side of burrows varied with the burrow host and the in- tered at all. fauna taxon considered (Fig. 3).Significant differences Throughout the investigation, specimens were in abundance between burrows and adjacent sediment recorded to the lowest possible taxonomic level, but were usually due to higher densities in the burrows. only Polychaeta and Platyhelminthes could be treated Scopimera inflata.Densities of infauna in the bur- at the species level. rows of sand bubbler crabs were not significantly dif- Fauna1 densities were compared for significant dif- ferent from adjacent sediment (Table 1). Only Platy- ferences between burrows and adjacent sediment and helminthes were significantly more abundant in the between experimental treatments, using the non- burrows, due to a higher abundance of predatory parametric Mann-Whitney U-test. In some cases, spe- platyhelminth species. A total of 11 platyhelminth cies similarities were compared using the index of species was recorded in the burrows compared to 6 in similarity (QS) (Serrensen 1948). Community composi- ambient sediment (QS = 0.59). Gastrotricha were only tions were assessed using the PRIMER software pack- located in the burrows. The meiofauna community in

burrow of: Scopimerainflata Uca spp Lingulaanatina Callianassa australiensis -0 E -0 .c -a Flg. 3 Schematic drawlng of m the studled burrow types and U the observed effects on melo- -C 30 fauna Both Scopimera inflata a, and Vca spp are ocypod~d E U crabs whlch excavate thelr a, (O burrows The animals are not drawn to scale. Melofaunal me~ofauna abundances are glven as me- ?E 5] l XI l,1500 ? shadingd~anvalues, refer columns to burrows, wlth thoselight o , , E wlth dark shadlng to adjacent 25 ,l 250 g sed~mentMeiofauna taxa that k 7 were sign~f~cantlymore abun- v i, 5 dant in the burrows are ~llus- c- 0 0 trated See 'Results' for further Nov May details Dittmann: Macrobenthic burrows in tropical tidal flats 123

Table 1. Infaunal densities (individuals 1.77 cm-2, 0-5 cm depth, n = 6 A total of 36 platyhelminth species was found each) in burrows of the Scopimera inflata(Hinch- at this site and the species distfibution was simi- inbrook Channel, 19 November 1988) and of fiddler crabs Uca spp. lar in burrows and adjacent sediment, In May, (Haughton Estuary, 23 August 1991). and in sediment adjacent to their burrows. Values are medians with ranges; ns = not significant (p > 0.05) abundances of grazing platyhelminths were nificantly higher in adjacent sediment (Table 2). Burrows Adjacent Mann-Whitney The sediment horizon from 5 to 10 cm depth, sediment U-test which was sampled additionally in May, con- tained only 1 to 6% of the meiofauna numbers of Scopimera inflala Permanent meiofauna the entire sampling depth (0 to 10 cm). Primarily Total 33 (13-67) 26 (11-35) ns nematodes occurred in the deeper sediment Nematoda 13 (8-39) 5 (7-13) ns layers, and significantly more of these were Copepoda 9 (4-25) 10.5 (1-20) ns Platyhelminthes 3 (1-5) 1 (0-5) p c 0.05 found in the ambient sediment than in the bur- Predators 2.5 (1-5) 0 p c 0.05 rows in this horizon (Table 2). Here, a gastro- Gastrotr~cha 0.5 (0-1) 0 p < 0.05 trich, a gnathostomulid and platyhelminths of the Polychaete larvae 2 (0-1 l) 0.5 (0-2) ns genus Retronectes were also found. Uca spp. Other infauna examined (small macrofauna Permanent meiofauna Total 45 (9-140) 17.5 (10-49) p < 0.05 retained on the 125 pm mesh) were more numer- Nematoda 42 (9-135) 12.5 (9-48) p < 0.05 ous in the burrows on the first sampling date Copepoda 2 (0-6) 2 (0-6) ns (Table 2). Twelve polychaete species were Ostracoda 1 (0-3) 0 p c 0.01 Oligochaeta 3 (0-5) 1 (0-4) ns distinguished at this site (llsted by decreasing abundance: Armandia intermedia, Ancistrosylhs burrows of S. inflata did not differ Table 2. Infaunal densities (individuals 5 cm-2, 0-5 cm; in May also 5-10 cm; from the ambient community when n = 6 each for 19 November 1988, n = 5 each for 4 May 1989; Hinchinbrook with multivariate analyses Channel) in burrows of Lingulaanatina and sediment adjacent to the burrows. Values are medians with ranges; ns = not significant (p > 0.05) (ANOSIM: R = 0.04, p = 0.307). Uca spp. Nematoda, accounting for Burrows Adjacent Mann-Whitney about 90% of meiofauna at this site, sediment U-test were responsible for the difference in infaunal densities between burrows November and adjacent sediment (Table 1). Permanent meiofauna Total 384 (263-680) 538 (372-650) p < 0.05 Other taxa were represented by only a Nematoda 350 (190-630) 480 (280-555) ns few individuals. Ostracoda were only Copepoda 15 (4-45) 25.5 (17-46) p < 0.05 found in burrow samples (a total of 8 Platyhelminthes 16.5 (10-34) 18.5 (14-28) ns Ostracoda 4.5 (0-9) 8 (0-11) ns individuals). As in the case of Scopimera Kinorhynchia 0 (0-2) 2 (1-8) p < 0.01 inflata, no community difference could Temporary meiofauna be detected between burrows and Total 2 (0-5) 2 (0-9) ns ambient sediment with multivariate Macrofauna Total 14 (7-16) 6 (1-11) p < 0.01 analyses (ANOSIM: R = 0.09, p = 0.210). Oligochaeta 2.5 (0-6) 0 (0-2) p < 0.05 Lingula anatina. Here, the compari- Polychaeta 12 (2-13) 5 (1-10) p < 0.01 son was repeated before (November) Armandiaintermedia 6.5 (2-11) 0 (0-1) p < 0.001 and after (May) the wet season and Crustacea 0.5 (0-1) 0 p < 0.05 yielded different results on each sam- May pling occasion. Meiofaunal densities Permanent meiofauna Total 377 (255-542) 169 (150-259) were higher in adjacent sediment on Nematoda 0-5 cm 350 (240-450) 150 (120-230) the first sampling date and higher in Nematoda 5-10 cm 3 (2-5) 9.5 (1-17) the burrows on the second (Table 2). In COpe poda 20 (10-80) 10 (7-20) Platyhelminthes 6 (3-9) 9 (6-15) November, no separate meiofauna Grazers 3 (0-5) 8 (4-10) communities could be distinguished Temporary meiofauna inside and outside of burrows, where- Total 1 (0-4) 0 (0-1) as in May separate communities were Macrofauna Total 5 (5-15) 7 (5-9) identified by clustering (Fig. 4 b, d) Oligochaeta 1 (0-2) 1 (1-2) and MDS ordination (not shown) Polychaeta 4 (2-12) 4 (3-7) (ANOSIM: R = 0.72, p = 0.008). - 124 Mar Ecol Prog Ser 134: 119-130, 1996

b"EI0FAUNA community composition in the burrows November 1988 differed from that in the adjacent sedi- ment (Fig. 5) and this difference was sig- nificant (ANOSIM: R = 0.66, p = 0.008). On the species level, 15 platyhelminth species occurred in the burrows com- pared to 13 outside, with 9 species in common, which resulted in a low species similarity between the 2 sample sets (QS = 0.56). The densities of 6 ind~vidual species (Myozona sp., Vannucia sp., Du- plominona sp., Prosenata indet., Gyra- trix sp., Carcharodorhynchus sp.) and of all predatory Platyhelminthes were significantly higher in the burrows (Table 3). However, the difference in the total platyhelminth community between POLYCHAETA 0 burrows and ambient sediment was only (cl November 1988 (U)May 1989 slight (ANOSIM: R = 0.35, p = 0.008).

l l I

Exclusion experiment

The exclusion of callianassid shrimps was effective and the density was sig- nificantly reduced, down to 6 shrimps m-' compared to 150 shrimps m-2 at the control sites (p < 0.001). No differences were detected in the density of Callia- nassa australiensis between control sites and ambient areas (165 shrimps m-2). inn.U- I- s s s s s s B B 8 8 B B S S 8 S S S B B 8 B The exclusion sites could still be d~stin- guished after 1 yr, when on average 20 Flg. 4. Cluster analysis of community differences in burrows of Llngula analina (B) and adjacent sediment (S): (a, b) for meiofauna (phylum level); m-2 were counted at the exclu- (c, d) for polychaetes (species level) sion sites compared to 121 at the control sites (p < 0.001). parva, Nereis sp , Sphaerosyllis sp., Table 3. Infaunal densltles (individuals 5 cm-2, 0-5 cm, n = 5 each) in burrows of Exogone sp., Maldanidae indet.. Capi- Callianassa australiens~sandin sediment adjacent to the burrows. Hauyhton Es- tella sp., Polydora sp., Syllidae indet., tuary. 17 April 1989. Values are medians with ranges; ns =not significant (p> 0.05) Schistomeringos sphairatolobus, Prio- nospio sp., Pygospio sp.) and in Burrows Adjacent Mann-Whitney November this community was clearly sediment U-test different inside and outside of the Permanent meiofauna Llngula anatina burrows (Fig. 4c) Total 305 (180-362) 131 (82-200) p < 0.01 (ANOSIM: R = 0.79, p = 0.002). On the Nematoda 190 (130-230) 100 (60-120) p < 0.01 second sampling date, this was less Copepoda 44 (16-86) 25 (7-50) ns pronounced (Fig. 4d) (ANOSIM: R = Platyhelminthes 25 (19-46) 12 (7-16) p

0 - and Ostracoda were less pronounced. No consistent species-specific responses were detected among the Platyhelminthes, but grouped by feeding mode, graz- > - t ing taxa were significantly more abundant at the con- tt q - trol sites at Weeks 6 (p < 0.05), 18 (p < 0.01) and 53 (p 1- 0.05). The vertical distribution showed that meiofaunal r- (I) densities in the exclusion treatments were reduced over V, 50- the sediment depth sampled (Table 6). Eighty-three + tt percent of the Platyhelminthes occurred in 0-1 cm sedlment depth and only a few copepod specimens

53wereand wk, control found the inmeiofaunalsites the weredeeper distinctlycommunities sediment different layer. of the After (Fig. exclusion 18 6b, and c)

(ANOSIM: Week 18: R = 0.79, p = 0.002; Week 53: R = loo 0.43, p = 0.004). i SSSSBSBBBB :n-zTh The macrofauna showed significantly reduced den- Fig. Cluster analysis of community differences sities in the exclusions only after 1 wk and after 1 yr, in (phylun~level) between burrows of Caihanassa australiensis both cases due to amphipods (Table 5).After 1 Yr! (B)and adjacent sediment (S) bivalve recruitment was detected at the exclusion sites. The 12 polychaete species recorded in this area during the study occurred in low numbers and their Occasionally, tubes of a terebellid polychaete (Loima distribution patterns did not react to the shrimp exclu- sp.), fecal pellets of Heteromastus sp. and tracks of sions. However, the species similarity between exclu- echiurids, snails, mudskippers and fiddler crabs were sion and control sites decreased from QS = 0.91 after seen at the exclusion sites, just as in the ambient areas and at the control Table 4. Meiofaunal densities [individuals 3.69 cm-'. 0-5 cm depth) in experi- sites. This revealed that the implanted mental exclusions of ~alljanassaaustraliensis and in treatment controls; = 7 fly screen excluded only the callia- each for Weeks 1 to l l and n = 6 for Weeks 18 and 53 Values are medians with ranges; ns = not significant (p > 0.05) nassid shrimps, while none of the other tube- or burrow-building mac- Week Exclusion Control Mann-Whitney robenthic species was affected by the U-test experimental treatment. The sampling at Week 11 coincided with activity Total meiofauna 1 p < 0.01 of soldier crabs Mictyris longicarpus 6 p < 0.05 11 ns in the area and their feeding tracks 18 p < 0.001 covered the entire study area. 53 p < 0.01 The absence of shrimp burrows Nematoda 1 p < 0.05 had a strong effect on the meiofauna, 6 p < 0.05 whereas macrofauna, which occurred 11 ns in low individual numbers, displayed 18 p < 0.001 only moderate responses. Significant 53 p < 0.01 reductions in abundances of infauna Copepoda 1 were apparent from the very beginning (Tables 4 & 5),yet distinct communities could be identified by multivariate analyses only after several months of Platyhelminthes 1 exclusion (Fig. 6). On the sampling 6 date after 11wk, infaunal numbers 11 were lower than on previous dates and 18 the exclusion and control sites could 53 not be distinguished (Table 4). Ostracoda 1 For the meiofauna, and 6 11 copepod densities were significantly 18 lower at the exclusion sites. Differ- 53 ences in densities of Platyhelminthes 126 Mar Ecol Prog Ser 134: 119-130, 1996

Table 5. Macrofaunal densities (individuals 15 cm-'. 0-5 cm depth) in experi- DISCUSSION mental exclusions of Callianassa australiensis and in treatment controls; n = 7 for Weeks 1 to 11 and n = 6 for Weeks 18 and 53. Values are medians with ranges; ~h,investigated macrobenthic bur- ns = not significant (p > 0.05) rows influenced the species distribu- tion and abundance patterns of Week Exclusion Control Mann-Whitney infauna in the studied tropical tidal U-test flats and had a promotive effect on the Total macrofauna 1 benthos communities. Densities in 6 burrows exceeded ambient densities l I 1.5 to 2.5 times. At sites where Callia- 18 nassa a ustraliensis was experimentally 53 excluded, infaunal numbers were re- Polychaeta duced to about 55% of control vdlues. Nematodes were the taxon respond- ing most to the presence/absence of p < 0.05 burrows. The effects of burrows on infauna Amphipoda p < 0.05 ns varied with the type of burrow (Fig. 3). ns Burrows of Scopimera inflata and of p < 0.05 fiddler crabs did not host a distinctive p c 0.05 infaunal association. Burrows of Lin- n s gula anatina and Callianassa australi- ns ensis had a distinctive infaunal com- ns munity, yet this pattern was not ns p < 0.05 constant over time. In all cases, the burrows would have been a favour- Oligochaeta ns able habitat, as they offered a cooler p < 0.05 p < 0.05 environment than the sediment sur- face, where temperatures were usu- p c 0.05 ally about 28°C and could exceed 35°C (author's pers. obs.). The burrows pro- vided refuge from desiccation and 1 wk to 0.33 after 6 wk and 0.57 after 18 wk. The pres- may thus be a less harsh environment during the sum- ence or absence of shrimp burrows had no effect on mer months. This could explain some of the reported the macrofaunal community composition and the null variations in abundance patterns. It is not yet known hypothesis (no differences between treatments) could whether burrows also offer shelter from salinity not be rejected by ANOSIM. changes following seasonal floods or monsoonal rains.

(a1week 6

C

%=E E

E E

Fig. 6 MDS of the meiobenthic community (phylum level) in the course of the experiment E: experimental exclusion of Calha- nassa austrahensis; C:control sltes. Stress values are: (a) 0 02. (b) 0.02, (c)0.06 Dittmann: Macrobenthic burrows in tropical tidal flats 127

Table 6. Depth distribution of meiofaunal densities (individuals 3.69 cm-2, n = 7) munity distinct from that in the adja- in experimental exclusions of Callianassa australiensis and treatment controls. cent sediment. Yet, the significantly Values are medians with ranges; ns = not significant (p> 0 05) increased density of nematodes in bur- rows of fiddler crabs recorded here is Depth Exclusion Control Mann-Whitney in accordance with studies on fiddler (cm) U-test crab burrows from other parts of the Week 1 world. Bell et al. (1978) reported Total meiofauna 0-1 83 (47-130) 104 (57-172) p < 0.05 increased meiofaunal abundances in 1-5 fiddler crab burrows in a salt marsh Nematoda 0-1 and they attributed the increase to a 1-5 more favourable food supply, follow- Week6 ing microbial decay of fecal pellets. Total meiofauna 0- 1 1-5 Similarly, DePatra & Levin (1989) Nematoda 0-1 found higher infaunal densities in fid- 1-5 17 (3-25) p < 0.05 dler crab burrows, but in addition to Week11 an increased food supply in the bur- Total meiofauna 0-1 57 (43-68) rows, they discovered that meiofauna 1-5 36 (18-50) were passively deposited in natural Nematoda 0-1 33 (27-40) i 1 1-5 25 (18-37) and artificial burrows. I observed fid- dler crabs plugging their burrows with a sediment disc before the incoming Posey (1986) found seasonal differences in the effect of arrived. Thus it is unclear whether passive deposi- Callianassa californiensis on amphipods. Thus, caution tion can explain the increased infaunal densities in the must be exercised when drawing inferences derived Uca burrows encountered here. Positive effects of fid- from single samplings. dler crab burrows are in contrast to the possible nega- The differences in infauna accommodated in bur- tive effect of Uca predation on meiofauna (Hoffmann rows may be related to specific attributes of the respec- et al. 1984). Dye & Lasiak (1986) yielded a 2- to 5-fold tive burrow type and to possible interactions between increase of meiofauna numbers in fiddler crab exclu- host and CO-residents.This is discussed below for each sion experiments set up on a tropical mud bank, but burrow type studied. they argued that microheterotrophs, not meiofauna. were the major food source of the crabs.

Burrows of ocypodid crabs Burrows of Lingula anatina Burrows of Scopimera inflata have a depth of about 30 cm, so that the crabs can reach the water level at Compared to ocypodid crabs, the brachiopod Lin- low tide (McCulloch & McNeill 1923-26). The burrows gula anatina is more sessile. On the sediment surface, of fiddler crabs also reach the water level. In salt its burrow openings are distinguishable as slot-like marshes, the burrowing activity of fiddler crabs can gaps. Lingulid brachiopods dig burrows with their increase the surface area by 59% (Katz 1980). At my valves (Thayer & Steele-Petrovic 1975, Morton & study site, several species of fiddler crabs coexisted Morton 1983). Once established, the burrows are and could not be distinguished by the burrow opening. maintained by vertical movements. Thus, disturbances Ocypodid crabs excavate their burrows anew at every along the burrow linings are less pronounced than in low tide (Altevogt 1957, Fielder 1970). The crabs use the case of ocypodids and the burrows are a more per- the burrows as refuges during high tide and as occa- sistent habitat for infauna. The higher densities and sional retreats during their activities on the surface at community differences of infauna recorded in the L. low tide (Reise 1985). Sand is cleared out of the burrow anatina burrows were not consistent over time and at and deposited as pellets on the surface before other present it remains unknown whether this reflects activities commence. As the water table falls during seasonal variation. The burrows may be optional sites low tide, S. inflata continually deepens the burrow for infauna, but more has to be known about species- (Fielder 1970). This process of excavation makes the specific responses before a conclusion can be drawn. burrows of Scopimera and Uca an unstable habitat for The polychaete Armandia intermedia, which was more associated fauna. The turnover of sediment due to crab abundant in the burrows, has been recorded through- activity may explain why the higher densities of some out the studied tidal flats (Dittmann unpubl.) and the meiofaunal taxa in the burrows did not result in a com- burrows are not an obligatory habitat for this taxon. Mar Ecol Prog Ser 134: 119-130, 1996

The finding of a Gnathostomulida and a Retronectes in were not analysed in my study, irrigation and fertiliza- the lower horizon of the adjacent sediment IS in con- ti.on of C. australiensis must be considered as possible trast to the recorded association of these taxa with tail factors enhancing meiofauna in the burrows. In the shafts of Arenicola marina (Reise 1981, 1987). experiment, densities of grazing Platyhelminthes were always higher at the control sites, which suggests an increased availability of benthic in the pres- Burrows of Callianassa australiensis ence of shrimps. This promotive effect might not have occurred in the other cases cited above, as the level The burrows of Callianassa australiensis are exten- of bioturbation attributable to Callianassa may vary sive and reach over 1 m in depth (Kenway 1981). with species (Griffis & Suchanek 1991). However, the Sampling of the lower realms of the burrows was methods available for calculating sediment turnover in methodologically impossible and throughout this Callianassidae vary widely, and comparisons of this study only the top parts of the burrows were consid- parameter are at present impossible (Rowden & Jones ered. Callianassid shrimps are mobile within their 1993). roomy burrow system, and all their activities take The sampling after 11 wk coincided with activity of place below ground. Meiofaunal densities were sig- soldier crabs Mictyris longicarpus. These crabs emerge nificantly higher in the burrows of C. australiensis at irregular intervals and pelletize the entire sediment and the absence of burrows led to a significant reduc- surface during their feeding treks, reducing meio- tion in meiofaunal densities at the exclusion sites and fauna1 numbers by predation (Dittmann 1993). The to different meiofaunal communities between the depth distribution (Table 6) showed that at all experi- exclusion and control sites. In the vertical dimension, mental sites, meiofaunal numbers were reduced in meiofauna was more numerous in the lower horizon the surface sediment layer, whereas densities in the of control sites than exclusions. The effect on the 1-5 cm horizon were still comparable to previous meiofauna became more and more pronounced in the values. This hints at a hierarchy of effects by macro- course of the experiment. fauna on smaller infauna. An experiment to study the The reduced abundance I recorded in the shrimp effects of various combinations of presence/absence of exclusions is comparable to the effect of lugworm shrimp and soldier crabs unfortunately failed following exclusions in an experiment conducted by Reise unfavourable weather conditions. (1983), from which he derived the importance of pro- Numbers of temporary meiofauna, however, were re- motive effects in tidal flat communities. But the results duced in the burrows of Callianassa australiensis and of this study are in contrast to accounts of reduced juvenile bivalves were almost exclusively recorded in meiobenthic and especially nematode densities in sediment adjacent to burrows and in exclusion sites. burrows of Callianassa trilobata from an intertidal When digging up sediment, shells of dead bivalves sandflat in Florida, USA (Dobbs & Guckert 1988), and <5 mm in size were often found at depths of about in burrows of Callianassa sp. in a subtidal reef lagoon 20 cm. Peterson (1977) described a competitive interac- (Alongi 1986). In an experimental study, Branch & tion for C. californiensis and the bivalve Sanguinolaria Pringle (1987) recorded reduced meiofaunal numbers nuttallii, in which he considered direct consumption with increasing densities of Callianassa kraussi, but and burial of newly recruited mussels to be the mecha- Dye & Furstenberg (1978) found a positive relationship nism of interaction. After 3 yr, the bivalves were well between the depth distribution of meiofauna and this established at his shrimp exclusion site (Peterson 1984). shrimp species. In a similar way, C, australiensis can inhibit the recruit- What could attract meiofauna to or repel them from ment of bivalves on the tidal flats of North Queensland. shrimp burrows? The extension of oxygenated sedi- Gammarid amphipods, which have already been ment surface to greater depths corresponds to an described by Kenway (1981) as commensals in the extension of habitat. Food supply for meiofauna is burrows of Callianassa australiensis, were absent from enhanced, as chlorophyll a values are higher in burrow my exclusion sites and thus seem to be obligate burrow linings (Dobbs & Guckert 1988),and in the presence of inhabitants. Callianassa kraussi more chlorophyll was found in This investigation showed that burrows of macro- deeper sediment layers than on the surface (Branch & benthic organisms in the tropics have promotive effects Pringle 1987). These authors also recorded higher bac- similar to those reported from other regions. In some teria numbers along the burrow linings, and along with cases, the interactions are complex and the burrow Frankenberg et al. (1967) they pointed out the trophic host can exert contradictory effects on associated significance of Callianassa fecal pellets Altogether, fauna. More studies are needed to elucidate the deeper this is a classical scenario for sediment amelioration realms of the thalassinidean burrows that still remain sensu Reise (1985).Although chlorophyll and bacteria cryptic. Dittmann: Macrobenthic burrows in tropical tidal flats

Note added in proof: Callianassa australiensis has recently Dobbs FC, Guckert JB (1988) Callianassa trilobata (Crus- been renamed Trypaea australiensis. tacea: Thalassinidea) influences abundance of melofauna and biomass, composition, and physlologic state of micro- Acknowledgements. This investigation was funded by a post- bial communities within its burrow. Mar Ecol Prog Ser 45: doctoral fellowship of the Deutsche Forschungsgemeinschaft 69-79 (DFG grant 111 02-Di 396/1-2). The Australian Institute of Dye AH, Furstenberg JP (1978) An ecophysiological study of Marine Science provided excellent research facilities and the meiofauna of the Swartkops Estuary. 2. The meio- special thanks to go the mangrove team, marine operations fauna: composition, distr~bution,seasonal fluctuation and and the crew of the research vessel 'Harry Messel' A big biomass. Zoologica Africana 13(1):19-32 thanks goes to J. van Kampen and A. Taplin, who could not Dye AH, Lasiak TA (1986) Microbenthos, meiobenthos and resist getting muddy and helped to set up the experiment fiddler crabs: trophic interactions in a tropical mangrove The help of numerous volunteers who joined my field trips sediment. Mar Ecol Prog Ser 32:259-264 over the years is very much appreciated. I am grateful to 1. Fielder DR (1970) The feeding behaviour of the sand crab Kroncke for providing access to the PRIMER software pack- Scopimera inflata (. Ocypodidae). J Zoo1 160: age and I thank her and K. Fabricius for discussions on the 35-49 manuscript Comments by anonymous reviewers helped to Frankenberg D, Coles SL, Johannes RE (1967) The potential improve the manuscript. trophic significance of Callianassa major fecal pellets. Limnol Oceanogr 12:113-120 Griffis RB, Suchanek TH (1991) A model of burrow architec- LITERATURE CITED ture and trophic modes in thalassinidean shrimp (Deca- poda: Thalassinidea). 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This article was submitted to the editor Manuscript first received: August 25, 1995 Revised version accepted: December 1, 1995